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Hydrological connectivity and Burkholderia pseudomallei prevalence in wetland environments: investigating rice-farming community’s risk of exposure to melioidosis in North-East Thailand

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Abstract

In our analysis of 136 water samples from wetland environments (rice paddies, natural wetland sites, man-made water bodies) in rural areas of North-East Thailand, Burkholderia pseudomallei was most prevalent in rice paddies (15 of the 30 positive sites). The high prevalence in the water of rice fields is indicative of the inherent vulnerability of farmers in rural agricultural areas in this area of Thailand and likely other locations in the tropics. Nearly all B. pseudomallei-positive sites were found within the vicinity of a large wetland associated with the Chi River, in the month of July 2014. Positive samples were found in water ranging in pH from 5.9 to 8.7, salinity ranging from 0.04 to 1.58 ppt, nitrate ranging from 0 to 10.8 ppm, and iron ranging from 0.003 to 1.519 ppm. Of these variables, only iron content was statistically higher in B. pseudomallei-positive versus B. pseudomallei-negative sites, suggesting that increasing concentrations of iron may encourage the growth of this bacterium, which is responsible for melioidosis. Our results, when combined with data from other published studies, support the notion that B. pseudomallei can exist in a wide range of environmental conditions. Thus, we argue that health safety education is a more appropriate means of addressing farmer vulnerability than chemical or physical alterations to fields at large scales. Further, it may be important to investigate melioidosis through transdisciplinary approaches that consider the complex social and ecological contexts in which the disease occurs.

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References

  • Amornchai, P., et al. (2007). Accuracy of Burkholderia pseudomallei identification using the API 20NE system and a latex agglutination test. Journal of Clinical Microbiology, 45(11), 3774–3776.

    Article  Google Scholar 

  • Baker, A., Tahani, D., Gardiner, C., Bristow, K. L., Greenhill, A. R., & Warner, J. (2011). Groundwater seeps facilitate exposure to Burkholderia pseudomallei. Applied Environmental Microbiology, 77(20), 7243–7246.

    Article  CAS  Google Scholar 

  • Baker, A., Mayo, M., Owens, L., Burgess, G., Norton, R., McBride, W. J. H., Bart, C. J., & Warner, J. (2013). Biogeography of Burkholderia pseudomallei in the Torres Straits island of northern Australia. Journal of Clinical Microbiology, 51(8), 2520–2525.

    Article  Google Scholar 

  • Baker, A. L., Ezzahir, J., Gardiner, C., Shipton, W., & Warner, J. M. (2015). Environmental attributes influencing the distribution of Burkholderia pseudomallei in northern Australia. PloS One, 10(9), e0138953.

    Article  Google Scholar 

  • Barnes, J. L., & Ketheesan, N. (2005). Route of infection of meliodosis. Emerging Infectious Diseases, 11, 638–639.

    Article  Google Scholar 

  • Bhengsri, S., Lertiendumrong, J., Baggett, H. C., Thamthitiwat, S., Chierakul, W., Tisayatocim, K., Tanwisaid, K., Chantra, S., & Kaewkungwal, J. (2013). Economic burden of bacteremic melioidosis in eastern and northeastern Thailand. Applied and Environmental Microbiology, 89(2), 369–373.

    Google Scholar 

  • Bouman, B. A. M., Humphrey, E., Tuong, T. P., & Barker, R. (2007). Rice and water. Advances in Agronomy, 92, 187–237.

    Article  CAS  Google Scholar 

  • Carpenter, S. R. (1996). Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology, 77(3), 677–680.

    Article  Google Scholar 

  • Chansrichavala, P., Wongsuwan, N., Suddee, S., Malasit, M., Hongsuwan, M., Wannapinij, P., Kitphati, R., Day, N. P. J., Michie, S., Peacock, S. J., & Limmathurotsakul, D. (2015). Public awareness of melioidosis in Thailand and potential use of video clips as educational tools. PloS One, 10(3), e0121311.

    Article  Google Scholar 

  • Chapin III FS, Eviner VT, Talbot LM, Wilcox BA, Magness DR, Brewer CA, Keebler DS, 2008. Disease effects on landscape and regional systems: a resilience framework. Ostfeld RS, Keesing F, Eviner V, eds, Infectious disease ecology: Effects of ecosystems on disease and of disease on ecosystems, Princeton: Princeton University Press.

  • Chaturongkasumrit, Y., Techaruvichit, P., Takahashi, H., Kimura, B., & Keeratipibul, S. (2005). Microbiological evaluation of water during the 2011 flood crisis in Thailand. Science of the Total Environment, 463-464, 959–967.

    Article  Google Scholar 

  • Chen, Y. S., Chen, S. C., Kao, C. M., & Chen, Y. L. (2003). Effects of soil pH, temperature and water content on the growth of Burkholderia pseudomallei Folia. Microbiologica, 40(2), 253–256.

    Article  Google Scholar 

  • Cheng, A. C., & Currie, B. J. (2005). Melioidosis: epidemiology, pathophysiology, and management. Clinical Microbiology Reviews, 18, 383–416.

    Article  CAS  Google Scholar 

  • Clermont-Dauphin, C., Suwannang, N., Grünberger, O., Hammecker, C., & Maeght, J. L. (2010). Yield of rice under water and soil salinity risks in the farmers’ fields in Northeast Thailand. Field Crops Research, 118, 289–296.

    Article  Google Scholar 

  • Dance, D. A. B. (2000). Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Tropica, 74, 159–168.

    Article  CAS  Google Scholar 

  • Draper, A. D. K., Mayo, M., Harrington, G., Karp, D., Yinfoo, D., Ward, L., Haslem, A., Currie, B. J., & Kaestil, M. (2010). Association of the melioidosis agent Burkholderia pseudomallei with water parameters in rural water supplies in northern Australia. Applied and Environmental Microbiology, 76(15), 5305–5307.

    Article  CAS  Google Scholar 

  • Fahy A, Mckew B, 2010. Microcosm. Timmis NK, McGenity, TJ, van der Meer JR, de Lorenzo V, ed, Handbook of hydrocarbon and lipid microbiology, Heidelberg: Springer.

    Google Scholar 

  • Finkelstein, R. A., Chulasamaya, M., Atthasanpana, P., Morris, J. H., Spertzel, R. O., (1965). Investigation of melioidosis in Thailand SEATO Medic Study no. 71, San Francisco: US Army-SEAT0 Medical Research Laboratory.

  • Haefele, S. M., Naklang, K., Harnpichitvitaya, D., Jearakongman, S., Skulkhu, E., Pomyen, P., Tabtim, S., Suriya-arunroj, D., Khunthasuvon, S., Kraisorakul, D., Youngskuj, P., Amarante, S. T., & Wade, L. J. (2006). Factors affecting rice yield and fertilizer response in rainfed lowlands of Northeast Thailand. Field Crops Research, 98, 39–51.

    Article  Google Scholar 

  • Hamad, M. A., Austin, C. R., Stewart, A. L., Higgins, M., Vasquez-Torres, A., & Voskuil, M. I. (2011). Adaptation and antibiotic tolerance of anaerobic Burkholderia pseudomallei. Antimicrobial Agents and Chemotherapy, 557, 3313–3323.

    Article  Google Scholar 

  • Hantrakun, V., Rongkard, P., Oyuchua, M., Premjit, A., Lim, C., Wuthiskanun, V., Day, N. P. J., Peacock, S. J., & Limmathurotsaku, D. (2016). Soil nutrient depletion is associated with the presence of Burkholderia pseudomallei. Applied and Environmental Microbiology, 82(24), 7086–7092.

    Article  CAS  Google Scholar 

  • Helsel, D. R. (2012). Things people do with censored data that are just wrong. In D. R. Helsel (Ed.), Statistics for censored environmental data using Minitab and R (2nd ed., pp. 1–10). John Wiley and Sons.

  • Howard, K., & Inglis, T. J. J. (2003). The effect of free chlorine on Burkholderia pseudomallei in potable water. Water Research, 37, 4425–4432.

    Article  CAS  Google Scholar 

  • Inglis, T. J. J., & Sagripanti, J. (2006). Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Applied Environmental Biology, 72(11), 6865–6875.

    Article  CAS  Google Scholar 

  • Inglis, T. J. J., & Sagripanti, J. L. (2007). Environmental survival, military relevance and persistance of Burkholderia pseudomallei report ECBC-TR-507. Nedlands: US Army Research Development and Engineering Command.

    Google Scholar 

  • Inglis, T. J. J., Garrow, S. C., Henderson, M., Clair, A., Sampson, J., O’Reilly, L., & Cameron, B. (2000). Burkholderia pseudomallei traced to water treatment plant in Australia. Emerging Infectious Diseases, 61, 56–59.

    Google Scholar 

  • Kaestli, M., Mayo, M., Harrington, G., Watt, F., Hill, J., Gal, D., & Currie, B. J. (2007). Sensitive and specific molecular detection of Bp, the causative agent of melioidosis, in the soil of tropical northeastern Australia. Applied and Environmental Microbiology, 73(21), 6891–6897.

    Article  CAS  Google Scholar 

  • Kaestli, M., Maya, M., Harrington, G., Ward, L., Watt, F., Hill, J. V., Cheng, A. C., & Currie, B. J. (2009). Landscape changes influence the occurrence of the melioidosis bacterium Burkholderia pseudomallei in soil in northern Australia. PLoS Neglected Tropical Diseases, 3(1), e364.

    Article  Google Scholar 

  • Kaestli, M., Schmid, M., Mayo, M., Rothballer, M., Harrington, G., Richardson, L., Hill, A., Hill, J., Tuanyok, A., Keim, P., Hartmann, A., & Currie, B. J. (2012). Out of the ground: aerial and exotic habitats of the melioidosis bacterium Burkholderia pseudomallei in grasses in Australia. Environmental Microbiology, 14(8), 2058–2070.

  • Kanai, K., & Kondo, E. (1994). Recent advances in biomedical sciences of Burkholderia pseudomallei Casonym: Pseudomonas pseudomallei. Japanese Journal of Medical Science & Biology, 47, 1–45.

    Article  CAS  Google Scholar 

  • Kao, C. M., Chen, S. C., Chen, Y. S., Lin, H. M., & Chen, Y. L. (2003). Detection of Burkholderia pseudomallei in rice fields with PCR-based techniques. Folia Microbiologica, 48(4), 521–524.

    Article  CAS  Google Scholar 

  • Kawasaki, J., & Herath, S. (2011). Impact assessment of climate change on rice production in Khon Kaen Province, Thailand. Journal of International Society for Southeast Asian Agricultural Science, 17(2), 14–28.

    Google Scholar 

  • Knappik, M., Dance, D. A. B., Rattanavong, S., Pierrer, A., Ribolzi, O., Davong, V., Silisouk, J., Vongsouvath, M., Newton, P. N., & Dittrich, S. (2015). Evaluation of molecular methods to improve the detection of Burkholderia pseudomallei in soil and water samples from Laos. Applied and Environmental Microbiology, 81(11), 3722–2727.

    Article  CAS  Google Scholar 

  • Leelarasamee, A. (2000). Melioidosis in Southeast Asia. Acta Tropica, 74(2–3), 129–132.

    Article  CAS  Google Scholar 

  • Limmathurotsakul, D., Wongratanacheewin, S., Teerawattanasook, N., Wongsuvan, G., Chaisuksant, S., Chetchotisakd, P., Chaowagul, W., Day, N. P., & Peacock, S. J. (2010). Increasing incidence of human melioidosis in Northeast Thailand. The American Journal of Tropical Medicine and Hygiene, 82(6), 1113–1117.

    Article  Google Scholar 

  • Limmathurotsakul, D., Thammasart, S., Warrasuth, N., Thapanagulsak, P., Jatapai, A., Pengreungrojanachai, V., Anun, S., Joraka, W., Thongkamkoon, P., Saiyen, P., Wongratanacheewin, S., Day, N. P. J., & Peacock, S. J. (2012). Melioidosis in animals, Thailand, 2006–2010. Emerging Infectious Diseases, 18(2), 325–327.

    Article  Google Scholar 

  • Limmathurotsakul, D., Kanoksil, M., Wuthiekanun, V., Kitphati, R., deStavola, B., NPJ, D., & Peacock, S. J. (2013a). Activities of daily living associated with acquisition of melioidosis in Northeast Thailand: a matched case-control study. PLoS Neglected Tropical Diseases, 7(2), e2072.

    Article  Google Scholar 

  • Limmathurotsakul, D., Dance, D. A. B., Wuthiekanun, V., Kaestil, M., Maya, M., Warner, J., Wagner, D. M., Tuanyok, A., Wertheim, H., Tan, Y. C., Mukhopadhyay, C., Puthucheary, S., Day, N. P. J., Steinmetz, I., Currie, B. J., & Peacock, S. J. (2013b). Systematic review and consensus guidelines for environmental sampling of Burkholderia pseudomallei. PLoS Neglected Tropical Diseases, 7(3), 1–11.

    Article  Google Scholar 

  • Limmathurotsakul, D., Wongsuvan, G., Aenensen, D., Ngamwilai, S., Saiprom, N., Rongkard, P., Thaipadungpanit, J., Kanoksil, M., Chantratita, N., Day, N. P. J., & Peacock, S. (2014). Melioidosis caused by Burkholderia pseudomallei in drinking water, Thailand, 2012. Emerging Infectious Diseases, 20(2), 265–268.

    Article  Google Scholar 

  • Limmathurotsakul, D., Golding, N., Dance, D. A. B., Messina, J. P., Pigott, D. M., Moyes, C. L., Rolim, D. B., Bertherat, E., Day, N. P. J., Peacock, S. J., & Hay, S. I. (2016). Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nature Microbiology, 1, 15008.

  • Mayo, M., Kaestil, M., Harrington, G., Cheng, A. C., Ward, L., Karp, D., Jolly, P., Godoy, D., Spratt, B. G., & Currie, B. J. (2011). Burkholderia pseudomallei in unchlorinated domestic bore water, tropical northern Australia. Emerging Infectious Diseases, 17(7), 1283–1285.

    Article  Google Scholar 

  • McRobb, E., Kaestil, M., Mayo, M., Price, E. P., Sarovich, D. S., Godoy, D., Spratt, B. G., & Currie, B. J. (2013). Short report: melioidosis from contaminated bore water and successful UV sterilization. The American Journal of Tropical Medicine and Hygiene, 89(2), 367–368.

    Article  Google Scholar 

  • Mekpruksawong, P., Chuenchooklin, S., & Ichikawa, T. (2012). The water quality and quality for conjunctive use in saline soil problem area. World Academy of Science, Engineering and Technology, 6(10), 803–810.

    Google Scholar 

  • Melioidosis.info (2013). Melioidosis in Thailand 2013 [Online]. Available at: http://www.melioidosis.info/download/20130922_143216%20melioidosis%20summary%20for%20moph%2020130907.pdf (accessed 22 October 2014).

  • Palasathien, S., Lertsirivorakul, R., Royros, P., Wongratanacheewin, S., & Sermswan, R. (2008). Soil physicochemical properties related to the presence of Burkholderia pseudomallei. Transactions of the Royal Society of Tropical Medicine and Hygiene, 102(S1), 5–9.

    Article  Google Scholar 

  • Peacock, S. J., Limmathurotsakul, D., Lubell, Y., Koh, G. C. K. W., White, L. J., Day, N. P. J., & Titball, R. W. (2012). Melioidosis vaccines: a systematic review and appraisal of the potential to exploit biodefense vaccines for public health purposes. PLoS Neglected Tropical Diseases, 6(1), 1–8.

    Article  Google Scholar 

  • Polthanee, A., & Promkhambut, A. (2014). Impact of climate change on rice-based cropping systems and farmers’ adaptation strategies in Northeast Thailand. Asian Journal of Crop Science, 6(3), 262–272.

    Article  Google Scholar 

  • Radkhe D. B., Davis, J. V., Wilde F. D. (2006). Specific electrical conductance, Wilde FD, ed, Field Measurement, USGS Survey Techniques of Water Resources Investigation, USGS: 3–22.

  • Risser, P. (1995). The status of the science examining ecotones. Bioscience, 45, 318–326.

    Article  Google Scholar 

  • Robertson, J., Levy, A., Sagripanti, J. L., & Inglis, T. J. J. (2010). The survival of Burkholderia pseudomallei in liquid medium. The American Journal of Tropical Medicine and Hygiene, 82(1), 88–94.

    Article  Google Scholar 

  • Sermswan, R. W., Royros, P., Khakhum, N., Wongratanacheewin, S., & Tuanyok, A. (2015). Direct detection of Burkholderia pseudomallei and biological factors in soil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 109(7), 462–468.

    Article  Google Scholar 

  • Smith, M. D., Wuthieknun, V., Walsh, A. L., & White, N. J. (1995). Quantitative recovery of Burkholderia pseudomallei from soil in Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene, 89(5), 488–490.

    Article  CAS  Google Scholar 

  • Sprague, L. D., & Neubauer, H. (2004). Melioidosis in animals: a review on epizootiology, diagnosis and clinical presentation. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 51(7), 305–320.

    Article  CAS  Google Scholar 

  • Strauss, J. M., Groves, M. G., Mariappan, M., & Ellison, D. W. (1969). Melioidosis in Malaysia. II. Distribution of Pseudomonas pseudomallei in soil and surface water. The American Journal of Tropical Medicine and Hygiene, 18(5), 698–702.

    Article  CAS  Google Scholar 

  • Suebrasri, T., Wang-ngarm, S., Chareonsudjai, P., Sermswan, R. W., & Chareonsubjai, S. (2013). Seasonal variation of soil environmental characteristics affect the presence of Burkholderia pseudomallei in Khon Kaen, Thailand. African Journal of Microbiology Research, 7(19), 1940–1945.

    Article  Google Scholar 

  • Summer, M. E., & Miller, W. P. (1996). Cation exchange capacity and exchange coefficients. In D. L. Sparks, A. L. Page, P. A. Helmke, & R. H. Loeppert (Eds.), Methods of soil analysis. Part 3, chemical methods (pp. 1201–1229). Madison: Soil Science Society of America, American Society of Agronomy.

    Google Scholar 

  • Suputtamongkol, Y., Hall, A. J., Dance, D. A., Chaowagul, W., Rajchanuvong, A., Smith, M. D., & White, N. J. (1994). The epidemiology of melioidosis in Ubon Ratchatani, Northeast Thailand. International Journal of Epidemiology, 23, 1082–1090.

    Article  CAS  Google Scholar 

  • Thai Meterological Department (2012). Weather outlook for Thailand during rainy season from June to October 2012. Available at: http://www.tmd.go.th/programs%5C%5Cuploads%5C%5Cforecast%5C%5C2012-05-29_Seasonal_EN_112920.pdf (accessed 15 December 2014).

  • Tong, S., Yang, S., Lu, Z., & He, W. (1996). Laboratory investigation of ecological factors influencing the environmental presence of Burkholderia pseudomallei. Microbiology and Immunology, 40, 451–453.

    Article  CAS  Google Scholar 

  • Vongphayloth, K., Rattanavong, S., Moore, C. E., Phetsouvanh, R., Wuthiekanum, V., Sengdouangphachanh, A., Phouminh, P., Newton, P. N., & Buiddon, Y. (2012). Burkholderia pseudomallei detection in surface water in southern Laos using Moore’s swab. The American Journal of Tropical Medicine and Hygiene, 86(5), 872–877.

    Article  Google Scholar 

  • Wagner, R. J., Boulger, Jr R. W., Carolyn, J. O., Smith, B. A. (2006). Guidelines and standard procedures for continuous water quality monitors: station operations, record computation, and data reporting. USGS Techniques and Methods. USA: US Geological Survey.

  • Wang-ngarm, S., Chareonsudjai, S., & Chareonsudjai, P. (2014). Physicochemical factors affecting the growth of Burkholderia pseudomallei in soil microcosm. The American Journal of Tropical Medicine and Hygiene, 90(3), 480–485.

    Article  CAS  Google Scholar 

  • White, N. J. (2003). Melioidosis. The Lancet, 361, 1715–1722.

    Article  CAS  Google Scholar 

  • Wiersinga, W. J., Poll, T. V. D., White, N. J., Day, N. D., & Peacock, S. (2006). Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nature Reviews Microbiology, 4, 272–282.

    Article  CAS  Google Scholar 

  • Wiersinga, W. J., Currie, B. J., & Peacock, S. J. (2012). Melioidosis. The New England Journal of Medicine, 367(11), 1035–1044.

    Article  CAS  Google Scholar 

  • Wongwanich, S., Chotanachan, P., Kondo, E., & Kanai, K. (1996). Multifactorial pathogenic mechanisms of Burkholderia pseudomallei as suggested from comparison with Burkholderia cepacia. The Southeast Asian Journal of Tropical Medicine and Public Health, 27, 111–118.

    CAS  Google Scholar 

  • Wuthiekanun, V., Dance, D. A., Wattanagoon, Y., Supputtamongkol, Y., Chaowagul, W., & White, N. J. (1990). The use of selective media for the isolation of Pseudomonas pseudomallei in clinical practice. Journal of Medical Microbiology, 33, 121–126.

    Article  CAS  Google Scholar 

  • Yang, H. M., Chaowagul, W., & Sokol, P. A. (1991). Siderophore production by Pseudomonas pseudomallei. Infection and Immunity, 59(3), 776–780.

    CAS  Google Scholar 

  • Yip, T. W., Hewagama, S., Mayo, M., Price, E. P., Sarovich, D. S., Bastian, I., Baird, R. W., Spratt, B. G., & Currie, B. J. (2015). Endemic melioidosis in residents of desert region after atypically intense rainfall in Central Australia, 2011. Emerging Infectious Diseases, 21(6), 1038–1040.

    Article  CAS  Google Scholar 

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Acknowledgements

This project was supported by grant R-109-000-134-112 from a MOE Tier II grant, National University of Singapore.

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  1. Institute of Water Policy, National University of Singapore, Singapore, Singapore

    C. Joon Chuah

  2. Department of Geography, National University of Singapore, Singapore, Singapore

    C. Joon Chuah, Esther K. H. Tan & Alan D. Ziegler

  3. Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

    Rasana W. Sermswan

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Chuah, C.J., Tan, E.K.H., Sermswan, R.W. et al. Hydrological connectivity and Burkholderia pseudomallei prevalence in wetland environments: investigating rice-farming community’s risk of exposure to melioidosis in North-East Thailand. Environ Monit Assess 189, 287 (2017). https://doi.org/10.1007/s10661-017-5988-1

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